Stimulus familiarity modulates functional connectivity of the perirhinal cortex and anterior hippocampus during visual discrimination of faces and objects

Frontiers in Human Neuroscience

Volumn 8, Issue MAR, 2014, Pages

  McLelland, Victoria C ^a   Chan, David ^a   Ferber, Susanne ^a,b   Barense, Morgan D ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ROTMAN RESEARCH INSTITUTE   (Canada)

Author keywords

Familiarity; Functional connectivity; Hippocampus; Perception; Perirhinal; Semantic memory

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN REGION; CONNECTOME; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; LEFT HEMISPHERE; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERCEPTION; PERCEPTIVE DISCRIMINATION; PERIRHINAL CORTEX; REACTION TIME; SEMANTIC DEMENTIA; SEMANTIC MEMORY; TASK PERFORMANCE; TEMPORAL LOBE; VISUAL DISCRIMINATION;

EID: 84896928197     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00117     Document Type: Article

References (79)

1. Anaki, D., and Bentin, S. (2009). Familiarity effects on categorization levels of faces and objects. Cognition 111, 144-149.doi: 10.1016/j.cognition.2009.01.002
2. Barense, M. D., Bussey, T. J., Lee, A. C. H., Rogers, T. T., Rhys Davies, R., Saksida, L. M., et al. (2005). Functional specialization in the human medial temporal lobe. J. Neurosci. 25, 10239-10246.doi: 10.1523/JNEUROSCI.2704-05.2005
3. Barense, M. D., Gaffan, D., and Graham, K. S. (2007). The human medial temporal lobe processes online representations of complex objects. Neuropsychologia 45, 2963-2974.doi: 10.1016/j.neuropsychologia.2007.05.023
4. Barense, M. D., Henson, R. N., and Graham, K. S. (2011). Perception and conception: temporal lobe activity during complex discriminations of familiar and novel faces and objects. J. Cogn. Neurosci. 23, 3052-3067.doi: 10.1162/jocn_a_00010
5. Barense, M. D., Henson, R. N., Lee, A. C. H., and Graham, K. S. (2010a). Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: effects of viewpoint. Hippocampus 20, 389-401.doi: 10.1002/hipo.20641
6. Barense, M. D., Rogers, T. T., Bussey, T. J., Saksida, L. M., and Graham, K. S. (2010b). Influence of conceptual knowledge on visual object discrimination: insights from semantic dementia and MTL amnesia. Cereb. Cortex 20, 2568-2582.doi: 10.1093/cercor/bhq004
7. Barense, M. D., Ngo, J. K. W., Hung, L. H. T., and Peterson, M. A. (2012). Interactions of memory and perception in amnesia: the figure-ground perspective. Cereb. Cortex 22, 2680-2691.doi: 10.1093/cercor/bhr347
8. Barsics, C., and Brédart, S. (2012). Recalling semantic information about newly learned faces and voices. Memory 20, 527-534.doi:10.1080/09658211.2012.683012
9. Bartko, S. J., Winters, B. D., Cowell, R. A., Saksida, L. M., and Bussey, T. J. (2007). Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J. Neurosci. 27, 2548-2559.doi:10.1523/JNEUROSCI.5171-06.2007
10. Binder, J. R., and Desai, R. H. (2011). The neurobiology of semantic memory. Trends Cogn. Sci. 15, 527-536.doi: 10.1016/j.tics.2011.10.001
11. Binney, R. J., Embleton, K. V., Jefferies, E., Parker, G. J., and Lambon Ralph, M. A. (2010). The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. Cereb. Cortex 20, 2728-2738.doi: 10.1093/cercor/bhq019
12. Bonner, M. F., Peelle, J. E., Cook, P. A., and Grossman, M. (2013). Heteromodal conceptual processing in the angular gyrus. Neuroimage 71, 175-186.doi: 10.1016/j.neuroimage.2013.01.006
13. Bruce, V., and Young, A. (1986). Understanding face recognition. Br. J. Psychol. 77, 305-327.doi: 10.1111/j.2044-8295.1986.tb02199.x
14. Bülthoff, I., and Newell, F. N. (2006). The role of familiarity in the recognition of static and dynamic objects. Prog. Brain Res. 154A, 315-325.doi: 10.1016/S0079-6123(06)54017-8
15. Bussey, T. J., and Saksida, L. M. (2002). The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur. J. Neurosci. 15, 355-364.doi: 10.1046/j.0953-816x.2001.01850.x
16. Bussey, T. J., and Saksida, L. M. (2007). Memory, perception, and the ventral visualperirhinal-hippocampal stream: thinking outside of the boxes. Hippocampus 17, 898-908.doi: 10.1002/hipo.20320
17. Cavanna, A. E., and Trimble, M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564-583.doi: 10.1093/brain/awl004
18. Chan, A. M., Baker, J. M., Eskandar, E., Schomer, D., Ulbert, I., Marinkovic, K., et al. (2011). First-pass selectivity for semantic categories in human anteroventral temporal lobe. J. Neurosci. 31, 18119-18129.doi: 10.1523/JNEUROSCI.3122-11.2011
19. Cowell, R. A., Bussey, T. J., and Saksida, L. M. (2010). Functional dissociations within the ventral object processing pathway: cognitive modules or a hierarchical continuum? J. Cogn. Neurosci. 22, 2460-2479.doi: 10.1162/jocn.2009.21373
20. Damasio, H., Tranel, D., Grabowski, T., Adolphs, R., and Damasio, A. (2004). Neural systems behind word and concept retrieval. Cognition 92, 179-229.doi:10.1016/j.cognition.2002.07.001
21. Davies, R. R., Graham, K. S., Xuereb, J. H., Williams, G. B., and Hodges, J. R. (2004). The human perirhinal cortex and semantic memory. Eur. J. Neurosci. 20, 2441-2446.doi: 10.1111/j.1460-9568.2004.03710.x
22. Devlin, J. T., and Price, C. J. (2007). Perirhinal contributions to human visual perception. Curr. Biol. 17, 1484-1488.doi: 10.1016/j.cub.2007.07.066
23. Ebisch, S. J. H., Babiloni, C., Del Gratta, C., Ferretti, A., Perrucci, M. G., Caulo, M., et al. (2007). Human neural systems for conceptual knowledge of proper object use: a functional magnetic resonance imaging study. Cereb. Cortex 17, 2744-2751.doi: 10.1093/cercor/bhm001
24. Fairhall, S. L., and Caramazza, A. (2013). Brain regions that represent amodal conceptual knowledge. J. Neurosci. 33, 10552-10558.doi: 10.1523/JNEUROSCI.0051-13.2013
25. Friston, K. J. (2011). Functional and effective connectivity: a review. Brain Connect. 1, 13-36.doi: 10.1089/brain.2011.0008
26. Gainotti, G. (2013). Laterality effects in normal subjects' recognition of familiar faces, voices, and names. Perceptual and representational components. Neuropsychologia 51, 1151-1160.doi: 10.1016/j.neuropsychologia.2013.03.009
27. Gauthier, I., and Tarr, M. J. (1997). Becoming a greeble expert: exploring mechanisms for face recognition. Vision Res. 37, 1673-1682.doi: 10.1016/S0042-6989(96)00286-6
28. Gesierich, B., Jovicich, J., Riello, M., Adriani, M., Monti, A., Brentari, V., et al. (2012). Distinct neural substrates for semantic knowledge and naming in the temporoparietal network. Cereb. Cortex 22, 2217-2226.doi: 10.1093/cercor/bhr286
29. Gorno-Tempini, M. L., and Price, C. J. (2001). Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. Brain 124, 2087-2097.doi: 10.1093/brain/124.10.2087
30. Gorno-Tempini, M. L., Price, C. J., Josephs, O., Vandenberghe, R., Cappa, S. F., Kapur, N., et al. (1998). The neural systems sustaining face and proper-name processing. Brain 121(pt 11), 2103-2118.doi: 10.1093/brain/121.11.2103
31. Graham, K. S., Barense, M. D., and Lee, A. C. H. (2010). Going beyond LTM in the MTL: a synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia 48, 831-853.doi: 10.1016/j.neuropsychologia.2010.01.001
32. Hodges, J. R., Patterson, K., Oxbury, S., and Funnell, E. (1992). Semantic dementia: progressive fluent aphasia with temporal-lobe atrophy. Brain 115, 1783-1806.doi: 10.1093/brain/115.6.1783
33. Jung, K., Ruthruff, E., and Gaspelin, N. (2013). Automatic identification of familiar faces. Atten. Percept. Psychophys. 75, 1438-1450.doi: 10.3758/s13414-013-0468-3
34. Kahn, I., Andrews-Hanna, J. R., Vincent, J. L., Snyder, A. Z., and Buckner, R. L. (2008). Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. J. Neurophysiol. 100, 129-139.doi: 10.1152/jn.00077.2008
35. Klein, I., Paradis, A.-L., Poline, J.-B., Kosslyn, S. M., and Le Bihan, D. (2000). Transient activity in the human calcarine cortex during visual-mental imagery: an event-related fMRI study. J. Cogn. Neurosci. 12, 15-23.doi:10.1162/089892900564037
36. Krishnan, A., Williams, L. J., McIntosh, A. R., and Abdi, H. (2011). Partial Least Squares (PLS) methods for neuroimaging: a tutorial and review. Neuroimage 56, 455-475.doi: 10.1016/j.neuroimage.2010.07.034
37. Lambert, S., Sampaio, E., Schieber, C., and Mauss, Y. (2002). Neural substrates of animal mental imagery: calcarine sulcus and dorsal pathway involvement an fMRI study. Brain Res. 2002, 176-183.doi: 10.1016/S0006-8993(01) 03232-2
38. Lee, A. C. H., Buckley, M. J., Pegman, S. J., Spiers, H., Scahill, V. L., Gaffan, D., et al. (2005a). Specialization in the medial temporal lobe for processing of objects and scenes. Hippocampus 15, 782-797.doi: 10.1002/hipo.20101
39. Lee, A. C. H., Bussey, T. J., Murray, E. A., Saksida, L. M., Epstein, R., Kapur, N., et al. (2005b). Perceptual deficits in amnesia: challenging the medial temporal lobe mnemonic view. Neuropsychologia 43, 1-11.doi:10.1016/j.neuropsychologia.2004.07.017
40. Lee, A. C. H., Scahill, V. L., and Graham, K. S. (2008). Activating the medial temporal lobe during oddity judgment for faces and scenes. Cereb. Cortex 18, 683-696.doi: 10.1093/cercor/bhm104
41. Lee, A. C. H., Yeung, L. K., and Barense, M. D. (2012). The hippocampus and visual perception. Front. Hum. Neurosci. 17:91.doi: 10.3389/fnhum.2012.00091
42. Leveroni, C. L., Seidenberg, M., Mayer, A. R., Mead, L. A., Binder, J. R., and Rao, S. M. (2000). Neural systems underlying the recognition of familiar and newly learned faces. J. Neurosci. 20, 878-886.
43. Levy, D. A., Bayley, P. J., and Squire, L. R. (2004). The anatomy of semantic knowledge: medial vs. lateral temporal lobe. Proc. Natl. Acad. Sci. U.S.A. 101, 6710-6715.doi: 10.1073/pnas.0401679101
44. Liang, J. C., Wagner, A. D., and Preston, A. R. (2012). Content representation in the human medial temporal lobe. Cereb. Cortex 23, 80-96.doi: 10.1093/cer-cor/bhr379
45. Libby, L. A., Ekstrom, A. D., Ragland, J. D., and Ranganath, C. (2012). Differential connectivity of perirhinal and parahippocampal cortices within human hippocampal subregions revealed by high-resolution functional imaging. J. Neurosci. 32, 6550-6560.doi: 10.1523/JNEUROSCI.3711-11. 2012
46. Litman, L., Awipi, T., and Davachi, L. (2009). Category-specificity in the human medial temporal lobe cortex. Hippocampus 19, 308-319.doi:10.1002/hipo.20515
47. Martin, V. C., Schacter, D. L., Corballis, M. C., and Addis, D. R. (2011). A role for the hippocampus in encoding simulations of future events. Proc. Natl. Acad. Sci. U.S.A. 108, 13858-13863.doi: 10.1073/pnas.1105816108
48. McGugin, R. W., Gatenby, J. C., Gore, J. C., and Gauthier, I. (2012). Highresolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc. Natl. Acad. Sci. U.S.A. 109, 17063-17068.doi: 10.1073/pnas.1116333109
49. McIntosh, A. R., Bookstein, F. L., Haxby, J. V., and Grady, C. L. (1996). Spatial pattern analysis of functional brain images using partial least squares. Neuroimage 3, 143-157.doi: 10.1006/nimg.1996.0016
50. McIntosh, A. R., Chau, W. K., and Protzner, A. B. (2004). Spatiotemporal analysis of event-related fMRI data using partial least squares. Neuroimage 23, 764-775.doi: 10.1016/j.neuroimage.2004.05.018
51. McIntosh, A. R., and Lobaugh, N. J. (2004). Partial least squares analysis of neuroimaging data: applications and advances. Neuroimage 23, S250-S263.doi: 10.1016/j.neuroimage.2004.07.020
52. McKeeff, T. J., McGugin, R. W., Tong, F., and Gauthier, I. (2010). Expertise increases the functional overlap between face and object perception. Cognition 117, 355-360.doi: 10.1016/j.cognition.2010.09.002
53. Moss, H. E., Rodd, J. M., Stamatakis, E. A., Bright, P., and Tyler, L. K. (2005). Anteromedial temporal cortex supports fine-grained differentiation among objects. Cereb. Cortex 15, 616-627.doi: 10.1093/cercor/bhh163
54. Murray, E. A., and Bussey, T. J. (1999). Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn. Sci. 3, 142-151.doi: 10.1016/S13646613(99)01303-0
55. Olson, I. R., McCoy, D., Klobusicky, E., and Ross, L. A. (2013). Social cognition and the anterior temporal lobes: a review and theoretical framework. Soc. Cogn. Affect. Neurosci. 8, 123-133.doi: 10.1093/scan/nss119
56. Olson, I. R., Plotzker, A., and Ezzyat, Y. (2007). The enigmatic temporal pole: a review of findings on social and emotional processing. Brain 130, 1718-1731.doi: 10.1093/brain/awm052
57. O'Neil, E. B., Cate, A. D., and Kohler, S. (2009). Perirhinal cortex contributes to accuracy in recognition memory and perceptual discriminations. J. Neurosci. 29, 8329-8334.doi: 10.1523/JNEUROSCI.0374-09.2009
58. O'Neil, E. B., Protzner, A. B., McCormick, C., McLean, D. A., Poppenk, J., Cate, A. D., et al. (2012). Distinct patterns of functional and effective connectivity between perirhinal cortex and other cortical regions in recognition memory and perceptual discrimination. Cereb. Cortex 22, 74-85.doi: 10.1093/cercor/ bhr075
59. Patterson, K., Lambon Ralph, M. A., Jefferies, E., Woollams, A., Jones, R., Hodges, J. R., et al. (2006). Presemantic cognition in semantic dementia: six deficits in search of an explanation. J. Cogn. Neurosci. 18, 169-183.doi:10.1162/jocn.2006.18.2.169
60. Patterson, K., Nestor, P. J., and Rogers, T. T. (2007). Where do you know what you know? The representation of semantic knowledge in the human brain. Nat. Rev. Neurosci. 8, 976-987.doi: 10.1038/nrn2277
61. Peterson, M. A., Cacciamani, L., Barense, M. D., and Scalf, P. E. (2012). The perirhinal cortex modulates V2 activity in response to the agreement between part familiarity and configuration familiarity. Hippocampus 22, 1965-1977.doi:10.1002/hipo.22065
62. Poppenk, J., Evensmoen, H. R., Moscovitch, M., and Nadel, L. (2013). Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 17, 230-240.doi:10.1016/j.tics.2013.03.005
63. Ranganath, C., and Ritchey, M. (2012). Two cortical systems for memory-guided behaviour. Nat. Rev. Neurosci. 13, 713-726.doi: 10.1038/nrn3338
64. Rogers, B. P., Morgan, V. L., Newton, A. T., and Gore, J. C. (2007). Assessing functional connectivity in the human brain by fMRI. Magn. Reson. Imaging 25, 1347-1357.doi: 10.1016/j.mri.2007.03.007
65. Rogers, T. T., Lambon Ralph, M. A., Garrard, P., Bozeat, S., McClelland, J. L., Hodges, J. R., et al. (2004). Structure and deterioration of semantic memory: a neuropsychological and computational investigation. Psychol. Rev. 111, 205-235.doi: 10.1037/0033-295X.111.1.205
66. Rorden, C., Karnath, H. O., and Bonilha, L. (2007). Improving lesion-symptom mapping. J. Cogn. Neurosci. 19, 1081-1088.doi: 10.1162/jocn.2007.19.7.1081
67. Schmolck, H., Kensinger, E. A., Corkin, S., and Squire, L. R. (2002). Semantic knowledge in patient H.M. and other patients with bilateral medial and lateral temporal lobe lesions. Hippocampus 12, 520-533.doi: 10.1002/hipo.10039
68. Schwarzbauer, C., Mildner, T., Heinke, W., Brett, M., and Deichmann, R. (2010). Dual echo EPI-the method of choice for fMRI in the presence of magnetic field inhomogeneities? Neuroimage 49, 316-326.doi:10.1016/j.neuroimage.2009.08.032
69. Squire, L. R., Stark, C. E. L., and Clark, R. E. (2004). The medial temporal lobe. Ann. Rev. Neurosci. 27, 279-306.doi: 10.1146/annurev.neuro.27.070203.144130
70. Squire, L. R., and Wixted, J. T. (2011). The cognitive neuroscience of human memory since H.M. Ann. Rev. Neurosci. 34, 259-288.doi: 10.1146/annurevneuro-061010-113720
71. Suzuki, W. A., and Amaral, D. G. (1994). Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350, 497-533.doi: 10.1002/cne.903500402
72. Taylor, K. I., Moss, H. E., Stamatakis, E. A., and Tyler, L. K. (2006). Binding crossmodal object features in perirhinal cortex. Proc. Natl. Acad. Sci. U.S.A. 103, 8239-8244.doi: 10.1073/pnas.0509704103
73. Trinkler, I., King, J. A., Doeller, C. F., Rugg, M. D., and Burgess, N. (2009). Neural bases of autobiographical support for episodic recollection of faces. Hippocampus 19, 718-730.doi: 10.1002/hipo.20556
74. Tyler, L. K., Chiu, S., Zhuang, J., Randall, B., Devereux, B. J., Wright, P., et al. (2013). Objects and categories: feature statistics and object processing in the ventral stream. J. Cogn. Neurosci. 25, 1723-1735.doi: 10.1162/jocn_a_00419
75. Tyler, L. K., Stamatakis, E. A., Dick, E., Bright, P., Fletcher, P., and Moss, H. (2003). Objects and their actions: evidence for a neurally distributed semantic system. Neuroimage 18, 542-557.doi: 10.1016/S1053-8119(02)00047-2
76. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289.doi: 10.1006/nimg.2001. 0978
77. Visser, M., Jefferies, E., and Lambon Ralph, M. A. (2010). Semantic processing in the anterior temporal lobes: a meta-analysis of the functional neuroimaging literature. J. Cogn. Neurosci. 22, 1083-1094.doi: 10.1162/jocn.2009. 21309
78. Wong, Y. K., Folstein, J. R., and Gauthier, I. (2012). The nature of experience determines object representations in the visual system. J. Exp. Psychol. Gen. 141, 682-698.doi: 10.1037/a0027822
79. Yonelinas, A. R. (2002). The nature of recollection and familiarity: a review of 30 years of research. J. Mem. Lang. 46, 441-517.doi: 10.1006/jmla.2002.2864